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DR. STEFAN C LÖHR (Orcid ID : 0000-0002-1242-552X) : Original Research Article

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Sediment microfabric records mass sedimentation of colonial cyanobacteria and extensive syndepositional metazoan reworking in Pliocene sapropels

Stefan C. Löhr1,2, Martin J. Kennedy1,2, Simon C. George1,2, Robyn J. Williamson3 & Huiyuan Xu1,4 1

Department of Earth and Planetary Sciences, Macquarie University, North Ryde, 2109, Australia 2

Macquarie University Marine Research Centre, Macquarie University, North Ryde, 2109, Australia 3

Sprigg Geobiology Centre & Department of Earth Sciences, University of Adelaide, Adelaide, 5005, Australia 4

School of Energy Resources, China University of Geosciences (Beijing), Beijing, 100083, China

Corresponding author: Stefan C. Löhr ([email protected])

ABSTRACT The sapropel record of the eastern Mediterranean provides unique insight into the primary climatic, oceanographic and biological drivers of organic carbon enrichment in marine sediments. The dominant source of organic matter, timing of oxygen-depletion at the sea floor, and extent of metazoan reworking of these deposits remain unclear. These questions are addressed by combining microbeam imaging with bulk and molecular geochemical characterisation of several Pliocene sapropels, revealing four microfacies which record distinct palaeoceanographic conditions, phytoplankton assemblages and degrees of postdepositional reworking. The most organic-rich, carbonate lean sapropel intervals consist of alternating 10-60 µm thick organic and detrital mineral laminae. Petrographic features This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1002/dep2.49 This article is protected by copyright. All rights reserved.

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consistent with a pelagic origin, δ15N 50 µm organomineral aggregates, interpreted as marine snow, whereas carbonate microfossil rich intervals record periods of nitrogen fixation and moderately increased primary production by a diverse assemblage of calcareous, organic-walled and siliceous plankton. The results presented here further show that burrowing by microscopic meiofauna impacted most sapropels, extending into seemingly laminated intervals below obvious disruption from burrowing macrofauna, indicating that metazoans influence organic carbon burial in oxygen-depleted settings even where physical displacement of sediment is not visible.

Keywords: cyanobacteria, Pliocene, sapropel, mass sedimentation, seafloor anoxia, organic matter source

INTRODUCTION Sapropels, organic carbon (OC)-rich, fine-grained sediments that are cyclically interbedded with organic-lean marls, are a conspicuous feature of the sedimentary record of the Mediterranean basin (Emeis et al., 2000). The sapropel record of the eastern Mediterranean, which extends from the Holocene (de Lange et al., 2008) into the late Miocene (early Tortonian; Schenau et al., 1999), has been studied in great detail to identify the primary climatic, oceanographic and biological drivers of organic carbon enrichment in marine sediments. The cyclical deposition of interbedded organic-rich sapropels and organic-lean marls in the eastern Mediterranean is closely timed with orbital forcing of the African monsoon (Rossignol-Strick, 1983) and has been related to increased freshwater influx resulting in density stratification and deep-water anoxia (for a current review see Rohling et al., 2015). It has been argued that the primary influences on the striking OC enrichment in sapropels relative to the interbedded organic-lean marls are i) increased phytoplankton production, most likely focussed in a deep chlorophyll maximum below an oligotrophic mixed layer, ii) inhibited deep-water renewal resulting in oxygen-depleted conditions conducive to OC preservation and iii) reduced clastic dilution (Van Os et al., 1994; Kemp et al., 1999; Nijenhuis et al., 1999; Schenau et al., 1999; Nijenhuis and de Lange, 2000; Struck et al., 2001; Rohling et al., 2006; Gallego-Torres et al., 2007; Marino et al., 2007; de Lange et al., 2008). There remains, however, much uncertainty about 1) the dominant

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primary producers contributing to sapropel formation, and how this varies within and between individual sapropels, 2) whether oxygen-depleted conditions developed abruptly or required long lead-up periods, and 3) the extent to which benthic reworking influences what is considered a classic ‘anoxic’ facies. The high abundance of laminae consisting of seasonal diatom bloom deposits, including laminae dominated by the mat-forming rhizosolenoid diatoms, in Pleistocene sapropel S5 (Kemp et al., 1999; Corselli et al., 2002; Moller et al., 2012) appeared to confirm early suggestions that mass-sedimentation of mat-forming diatoms is a critical component of sapropel formation (Sancetta, 1994), with average diatom Si/C ratios suggesting that diatoms can potentially account for the entire OC content of sapropel S5 and, more speculatively, perhaps also the highly enriched Pliocene sapropels (Kemp et al., 1999). Given that diatom-dominated ecosystems are characteristic of specific oceanographic settings, this would imply a limited set of conditions for sapropel formation. However, whereas molecular composition, δ13Corg > -23‰, hydrogen indices >>200 mg HC/g TOC and palynology/organic petrography of sapropels in numerous cores from the eastern Mediterranean confirm that the major fraction of organic matter (OM) derives from marine algal sources (Bouloubassi et al., 1999; Rinna et al., 2002; Menzel et al., 2003; 2005; Payeur et al., 2011), there is little petrographic, microfossil or biomarker evidence to suggest that diatoms are the dominant source of organic carbon in sapropels other than S5. Indeed, biomarker and δ15N ratios have been used to argue for significant organic carbon inputs by prymnesiophyte (Bouloubassi et al., 1999), dinoflagellate (Bouloubassi et al., 1999; Rinna et al., 2002; Menzel et al., 2003), eustigmatophyte (Menzel et al., 2005) or cyanobacterial (Meyers & Bernasconi, 2005; Gallego-Torres et al., 2011) primary producers in various Pleistocene and Pliocene sapropels, suggesting that the source of sapropel organic matter varies substantially through time and space. The identity of the phytoplankton assemblage(s) contributing to the formation of the highly OC-rich, laminated Pliocene sapropels, which are the closest analogues for the Mesozoic black shales (Emeis & Weissert, 2009), remains an open question with important palaeoceanographic implications. To date, unambiguous evidence for a diatom contribution to a Pliocene sapropel is known only for sapropel i172 at Site 969 (Kemp et al., 1998). The nature of the phytoplankton assemblage is also relevant to the debate around the rate, magnitude and distribution of basinal oxygen depletion. Early studies emphasized the importance of anoxic or sulphidic water column conditions for sapropel deposition, citing in particular the presence of isorenieratane and its derivatives (Passier et al., 1999a; Menzel et al., 2002), as well as framboidal pyrite (Passier et al., 1999b), as indicative of photic zone euxinia. High resolution multiproxy analyses of sapropel S5 suggest that basinal water-column anoxia requires 600-900 years to develop after deep-water renewal is inhibited by monsoon flooding and the onset of stratified conditions (Marino et al., 2007). However, a patchy but much more rapid onset of anoxia at the sea floor is indicated in several studies (Casford et al., 2003; Bianchi et al., 2006; Marino et al., 2007) where it is This article is protected by copyright. All rights reserved.

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attributed to the development of a thin anoxic bottom-water ‘blanket’ (Casford et al., 2003) in response to the patchy delivery of large aggregates of fast-sinking organic matter such as diatom mats (Bianchi et al., 2006). The extent to which this process was a factor in the extreme organic carbon enrichment of many Pliocene sapropels (up to 30% TOC) in the absence of clear evidence for mass-sedimentation of mat-forming diatoms is unknown but merits further investigation. Macrofaunal trace fossils such as Chondrites, recording post-depositional benthic reworking, are present in the upper portions of many sapropels (Shipboard Scientific Party, 1996c; Löwemark et al., 2006; Löhr & Kennedy, 2015), but comprehensive, syndepositional macrofaunal burrowing and emplacement of Zoophycus traces such as reported for two Pliocene sapropels at Site 969 is unusual (Shipboard Scientific Party, 1996c). Although benthic foraminiferal repopulation events indicative of episodic deep water ventilation are present in sapropels spanning the Pliocene to the Holocene (Rohling et al., 1993; Casford et al., 2003; Schmiedl et al., 2003; Jilbert et al., 2010; Rohling et al., 2015), and low-level benthic foraminiferal fauna are known to persist through the entire thickness of a smaller number of sapropels (Rohling et al., 1997; Jorissen, 1999; Casford et al., 2003), bottomwater conditions are generally considered too hostile to support a metazoan benthos. However, this view has begun to shift as recent work employing scanning electron imaging has revealed abundant sub-millimetre trace fossils in the upper third of two highly organicrich Pliocene sapropels at Site 969 (Löhr & Kennedy, 2015), demonstrating comprehensive syndepositional reworking of sapropels by a low-oxygen adapted meiobenthos. These observations are consistent with the ubiquitous presence and impact of sub-millimetre benthic metazoans in modern low-oxygen settings (Levin et al., 2003; Giere, 2008), although there are currently no other known examples in the sedimentary record. Determining whether meiofaunal reworking of sapropels is commonplace is essential given that meiofaunal activity exerts a significant influence on sediment biogeochemistry (Aller & Aller, 1992), including increased mineralisation of sedimentary OC (Rysgaard et al., 2000). Furthermore cryptic sediment mixing may result in averaging and reduced temporal resolution of a sedimentary archive that has been widely used to reconstruct decadal to centennial climatic and oceanographic variability. The present study demonstrates that sapropel microfabric preserves a high resolution record of palaeoceanographic conditions that can be accessed through systematic microbeam imaging, and provides important constraints on geochemical proxybased interpretations. Systematic electron microscopic, bulk and molecular geochemical characterisation of three Pliocene sapropel cycles at three geographically widely spaced sites in the Eastern Mediterranean Basin are combined to identify the range of sapropel microfabrics, mechanisms of organic matter enrichment, and the likely oceanographic controls resulting in their differentiation. Four microfacies are identified, and proposed to record distinct oceanographic conditions that control sediment composition via the balance between calcifying, siliceous and organic-walled primary producers, the timing of organic This article is protected by copyright. All rights reserved.

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matter deposition (episodic mass-sedimentation vs continuous), as well as the extent of post-depositional reworking by an evolving assemblage of benthic fauna. The combined analytical approach and interpretative framework developed here will facilitate efforts to reconstruct continuous, high resolution records of palaeoceanographic evolution and phytoplankton response associated with sapropel deposition. Future work will focus on producing these more continuous records and evaluating temporal and geographic differences in a basin-wide context.

MATERIALS AND METHODS Pliocene-aged sapropels corresponding to insolation cycles 278, 280, 282 and 284 in cores recovered during Ocean Drilling Program (ODP) Leg 160 (Eastern Mediterranean basin) at Sites 964, 969 and 967 were included in the study (Fig. 1). Previous work indicated that these represent a wide range of sapropel composition, ranging from relatively organicrich but carbonate-poor to relatively organic lean but carbonate rich intervals (Nijenhuis & de Lange, 2000; Wehausen & Brumsack, 2000), and therefore are likely to include a broad range of sapropel microfabric and organic matter sources that is representative of varying oceanographic conditions in the Eastern Mediterranean during the Pliocene. Sapropel nomenclature here follows Lourens et al. (1996) and Emeis et al. (2000), with sapropels designated according to the corresponding insolation (precession) cycle. Sites 964, 969 and 967 are distinguished by the suffix A, B and C (see Table 1). Samples were collected at 1 cm spacing in sapropels and immediately adjacent sediment, and at 5 cm spacing in the interbedded organic-lean marls (see Fig. 2). All the sampled sites were located on relative topographic highs when deposition of the sampled intervals occurred (Shipboard Scientific Party, 1996a, b, c). No evidence of gravity-flow deposits or of current winnowing or concentration such as erosional scours or traction was observed in the interval sampled for this study, so these sediments are considered to have been deposited from suspension as pelagic or hemipelagic deposits. Once received, all samples were visually assessed for evidence of lamination and macrobioturbation intensity. Visual assessment of the samples was complemented by information from ODP core description and core photographs. Samples received sufficiently intact to determine bedding were subsampled for SEM imaging, before the remaining sample material was milled in an agate ball mill (Fritsch Pulverisette 0). Total carbon (TC) content for each sample was measured in a Perkin Elmer 2400 Series II CHNS analyser. Inorganic carbon (IC, as carbonate) content was determined using the pressure-calcimeter method of Sherrod et al. (2002). The OC content was calculated by difference (TOC = TC - IC). Sapropel microfabric, including organic matter morphology and distribution, was determined at millimetre to sub-micron scales on a sub-set of the samples (see Fig. 2 for samples imaged) using either FEI Quanta 450 or FEI Teneo field emission


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scanning electron microscopes (SEM) equipped with backscattered electron (BSE) detectors and energy dispersive X-ray (EDX) analysers. Prior to imaging, samples were fixed onto SEM stubs with the imaged surface prepared perpendicular to bedding. Samples were oven-dried for 48 hours at 60 °C, gently dry ground until flat, cleaned with compressed nitrogen, ion milled until polished (Fischione 1060 Ar Ion Mill system) and coated with 5 nm Pt. The ion milling approach avoids the need to embed otherwise fragile samples in resin prior to polishing, preserving the original compositional contrast of the samples and facilitating the identification of sedimentary organic matter (Löhr et al., 2014; 2015). Organic matter was identified by its characteristic dark appearance in BSE images (low mean Z-number of organic matter), with EDX analyses of selected spots providing spectroscopic confirmation (Löhr et al., 2015). Organo-clay aggregates were identified where recognisable clay mineral flakes were embedded in organic material, and where EDX analyses revealed the presence of C, Si, as well as Al. Organic matter quantities in BSE images were estimated visually based on percent surface area of the examined surface. EDX elemental mapping (1µm step size) of selected samples served to identify the distribution of mineral phases including quartz (Si), feldspar silt (Si & Al), carbonate (Ca) and pyrite (Fe & S). Criteria including pellet size, morphology, composition relative to surrounding sediment, and relationship to other sedimentary features indicative of bioturbation (criteria are outlined in detail in Löhr & Kennedy, 2015) were used to identify and distinguish meiofaunal fecal pellets indicative of syndepositional reworking from pellets of pelagic origin, as well as the organisms likely to be responsible (Levin, 2003; Giere, 2008). A small subset of samples were further characterised using organic geochemical and stable isotope techniques in order to further constrain BSE imaging-based interpretations of organic matter source in each of the microfacies (sample depth indicated in Fig. 2). To this end, δ15N and δ13Corg values were determined for the most organic-rich sample of each sapropel interval. The δ13Corg values were measured on carbonate-free sample aliquots that were treated with 10% HCl, triple rinsed with deionised water and dried at 60 °C before analysis. The δ15N values were determined on untreated sample aliquots. All samples were run on a Nu Horizon IRMS coupled to an Eurovector EuroEA elemental analyser at the Stable Isotope Laboratory, University of Adelaide. Data are expressed in the conventional δ 15N and δ13C notations relative to air and PDB standards, respectively. Standardisation was based on in-house glycine (δ13C: −31.2‰, δ15N: +1.32‰), glutamic acid (δ13C: −16.72‰, δ15N: −6.18‰) and triphenylamine (δ13C: −29.3‰, δ15N: −0.54‰) standards which have been calibrated against several international standards. Long-term precision is > 400 µm; Fig. 6F) that is likely of benthic macrofaunal origin, here termed Type M. MF4B is restricted to carbonaterich, heavily macrofaunally bioturbated sapropel S282-C and likely reflects reworking of MF1-type sediments under less oxygen-depleted conditions relative to sapropels containing more abundant meiofaunal pellets. Both MF4A and MF4B are overprinted by macroscopic Chondrites isp. trace fossils, produced by large macrofauna burrowing downwards from overlying marls after sapropel deposition had ceased and infilled by material from the overlying marl. The preservation of sharp burrow boundaries and infill derived from the This article is protected by copyright. All rights reserved.

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overlying marl shows that the Chondrites traces post-date sapropel deposition and meiofaunal reworking, and indicates that meiofaunal reworking of the upper sapropels is a syndepositional process. The organic-rich part of sapropel S278-B is classified here as Microfacies 4B, although it lacks Type M faecal pellets. This sapropel features macrofaunal burrows throughout so that the microfabric is a product of macrofaunal reworking rather than depositional processes.

Organic geochemistry The molecular geochemical analyses specifically targeted a representative of each microfacies with the aim of further constraining the sources of organic matter, in particular the contribution of diatoms and cyanobacteria as indicated by the presence of highly branched isoprenoids (HBIs; Sinninghe Damsté et al., 2004) and 2α-methylhopanes (Summons et al., 1999), respectively. Due to small sample size, multiple vertically adjacent samples were aggregated prior to solvent extraction (Table 4). The marl below S284-C was analysed to assess the background HC content in the core, and as it was very lean it is not discussed further. The aliphatic fractions of the three sapropel samples are dominated by n-alkanes ranging in molecular weight from C11 to C35 (Fig. 7A). There are anomalously elevated amounts of n-C12, n-C14, n-C16 and n-C18 in all three samples, which were not seen in laboratory blanks nor in freshly extracted material from similar sapropels (Rullkötter et al., 1998), so are attributed to contamination during core storage or transport. Higher molecular weight n-alkanes maximise at n-C31 or n-C29, and have a strong odd-over-even carbon number predominance (Table 4). Pristane/phytane is 0.6–0.8, and a large amount of lycopane was detected in the three sapropels (Fig. 7A). Isorenieratene or its derivatives were not detected in the aromatic fractions. The sample from sapropel S284-C (MF1) contains a small amount of the saturated C25 HBI (Fig. 7B) (Robson & Rowland, 1986), but the C20 and C30 HBIs were not detected. C25 HBI is absent from the other two sapropels (MF 2 and 3). Two large peaks (a and b) eluting between n-C21 and n-C22 in sapropel S284-C (Fig. 7B) have very similar mass spectra, with a molecular ion at m/z 348, and large m/z 263 (M+-85) and m/z 179 (M+-169) ions (Fig. 7C). Peaks c, d, e and f also have a molecular ion at m/z 348, but have a prominent m/z 210 (M+138) ion (Fig. 7D). These compounds have been identified before in Site 964 (Rullkötter et al., 1998) and Site 969 (Bouloubassi et al., 1998) sapropels and may be C25 bicyclic alkanes, but their structural identity remains unknown (Simon Belt, pers. comm.). Additionally, by monitoring m/z 348 and m/z 346 it was possible to identify the presence of C25 HBI dienes and trienes in sapropel S284-C (MF1), respectively (Fig. 7B). None of these C25 bicyclic and unsaturated HBIs were detected in sapropels S280-C or S284-A (MF 2 and 3). Sapropel S280C contains a large peak (j) eluting just after n-C23 in the TIC (Fig. 7A and E), which has a


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molecular ion at m/z 380 and prominent m/z 115, 169, 239 and 267 ions (Fig. 7F). Comparison with the literature (Kohnen et al., 1990) suggests that this peak, and two smaller slightly earlier eluting peaks (h and i), may be C25 HBI thiolanes or related compounds, although this remains uncertain. Biomarkers present in the aliphatic fraction of the three sapropels include hopenes, hopanes (Fig. 7G) and sterenes (Fig. 7H), but few steranes are present. The hopanes are dominated by 17β-22,29,30-trisnorhopane and the C29–C31 17(β),21(β) isomers. There is significant variation in the relative amounts of the C30 hopene isomers between the samples (Fig. 7G). The identified sterenes include cholest-4-ene and C28 and C29 sterenes and steradienes, and there are also significant differences in their distributions between the samples (Fig. 7H). The predominance of unsaturated and thermally unstable saturated biomarkers shows that the organic matter in the sapropels is very well preserved and not thermally altered. The sulphur-bound lipids released by Raney nickel de-sulphurisation are dominated by large unresolved complex mixtures and have different distributions of biomarkers compared to the free hydrocarbon fractions. No saturated C20, C25 or C30 HBIs or unsaturated HBI homologues were detected in the sulphur-bound fraction of the three sapropel samples. However, small amounts of 2α-methylhopanes are present in all three sapropel sulphur-bound fractions (Fig. 7I), whereas these biomarkers are not present in the free aliphatic fractions (Table 4).

DISCUSSION The cyclical, decimetre-scale pattern of organic enrichment characteristic of the Mediterranean sapropels is expressed as four distinct microfacies which record distinct palaeoceanographic conditions associated with sapropel deposition. When considered together with their compositional, isotopic and molecular properties these identify (1) the main primary producers and the mechanism of sediment/OC delivery to the sea floor, (2) how these are linked to the onset of sea-floor anoxia, and (3) the extent to which these classic anoxic facies were the subject of post-depositional metazoan reworking.

Origin of organic matter in laminated, high TOC sapropel intervals The most OC-rich intervals of sapropels S282-A, S280-B, S282-B and S280-C are characterised by a striking, strongly laminated microfabric (MF2) comprising OC-lean, detrital mineral laminae alternating with discontinuous organic laminae largely devoid of detrital minerals (Fig. 4). A similar laminated fabric has been reported for Pliocene sapropel i172 by Kemp et al. (1998). Although lamination is one of the most readily recognised sedimentary features, the compositional variation defining laminae is rarely identified,


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making the origin and significance difficult to determine. The microbeam imaging of laminae allows variation at this scale to be determined (Brodie & Kemp, 1995; O'Brien, 1996; Pike & Kemp, 1996; Kemp et al., 1998; Pilskaln & Pike, 2001). Two very different processes can potentially account for the compositional variation in these laminae: (1) benthic microbial mat growth punctuated by episodic sedimentation; (2) episodic mass-sedimentation of matforming or colonial pelagic plankton against a hemipelagic/pelagic background rain.

A pelagic origin for the organic laminae Alternating organic-rich and organic-lean laminae 2000 m at all three study sites rule out the presence of photoautotrophic benthic mats, leaving the possibility of heterotrophic or chemoautotropic microbial mats. Two criteria are commonly used to distinguish benthic microbial mats from pelagic accumulations, (1) organic laminae with a crinkly wavy appearance that are continuous on the millimetre to centimetre scale (O'Brien, 1996; Schieber, 2007), and (2) dispersed siltsized grains and lenses of detrital material embedded in the organic laminae reflecting deposition of discrete grains on a mat surface with subsequent overgrowth of the grains by the mat (Oschmann, 2000; Gorin et al., 2009). Indeed, the relatively longer time-frames represented by mat growth compared with short-lived episodic sedimentation of detrital material in this scenario requires a concentration of silt-size material (interpreted as Saharan dust in the Mediterranean; Larrasoaña et al., 2008) in the organic laminae relative to the detrital laminae. On the basis of these criteria, the discrete organic laminae that characterise MF2 are more likely to be of pelagic than benthic origin. The organic laminae are mainly non-parallel (Fig. 4A), are discontinuous at the millimetre scale and, although they are wavy, they do not have the crinkly appearance that has been attributed to benthic microbial mats in past studies (Schieber, 2007). Silt grains of likely aeolian origin are more common in inorganic laminae (Fig. 4B), which is inconsistent with reduced rates of sedimentation associated with benthic microbial mat growth which would predict a greater concentration in the slowly accumulating mat intervals. In addition, the scattered presence of shorter (< 200 µm) and more uniformly thick but otherwise identical discontinuous laminae in MF3 (Fig. 4D) implies that the more continuous organic laminae in MF2 are composites produced by mass This article is protected by copyright. All rights reserved.

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sedimentation of smaller mat fragments or colonies, and that these become amalgamated during compaction (see below).

Organic laminae record pelagic colonial cyanobacterial input, not mat-forming diatoms Episodic mass-sedimentation of mat-forming or colonial plankton can contribute disproportionately to particle flux to the deep sea (La Rocha & Passow, 2007), delivering the equivalent of the annual average carbon flux in the course of a few days to a few weeks (Beaulieu, 2002). Such pulses of phytodetritus to the sea floor have been described in all ocean basins (La Rocha & Passow, 2007) and are usually associated with seasonal phytoplankton blooms or breakdown of water column stratification by convective mixing (Kemp et al., 2000). In both cases the rapidly sedimented phytodetritus is typically dominated by diatoms, which form an organic-rich ‘fluff’ layer at the sea floor (Beaulieu, 2002) onto which subsequent lithogenic hemipelagic material is deposited (Pilskaln & Pike, 2001). The abundance of well-preserved diatom microfossils at ODP Site 971 indicates that seasonal mass-sedimentation of mat-forming rhizosolenoid diatoms was a dominant contributor to OC export during deposition of the laminated late Quaternary sapropel S5 (Kemp et al., 1999), and a similar scenario has been proposed for the highly OC-enriched Pliocene-aged sapropels (Kemp et al., 1998). The molecular geochemical results presented here demonstrate the input of microbial organic matter (presence of hopanes and hopenes), eukaryotic organic matter that is probably dominated by marine algae (presence of sterenes), and higher plant organic matter (long chain n-alkanes with a strong odd-overeven carbon number predominance), consistent with previous studies (Bouloubassi et al., 1999; Menzel, et al., 2005). The presence of cyanobacteria is suggested but not demanded by the presence of sulphur-bound 2α-methylhopanes (Rashby et al., 2007; Welander et al., 2010; Ricci et al., 2014). There is, however, no direct evidence for diatom-dominated productivity which could account for the formation of organic-rich laminae which are characteristic of these most OC-rich intervals.

The samples imaged contain no identifiable diatom remains. Indeed, it appears that the great majority of Pliocene sapropels studied to date do not contain diatom remains, with a few exceptions such as the presence of poorly preserved (etched) diatom remains in sapropel i172 at Site 969 (Kemp et al., 1998). The absence of diatom remains at other sapropel i172 sites (e.g. 967), and Pliocene-aged eastern Mediterranean sapropels more broadly, has been attributed to quantitative dissolution of diatom remains rather than a lack of diatom input. There is no doubt that the Si undersaturated waters of the Mediterranean are highly corrosive to biogenic opal (Krom et al., 1991; Kemp et al., 1999), so that abundant diatom remains are generally only preserved where bottom waters are buffered from the open Mediterranean (e.g. anoxic brine basins with elevated Si concentration (de Lange et This article is protected by copyright. All rights reserved.

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al., 1990; Erba, 1991). However, the biomarker data argues against a significant diatom contribution to the laminated Pliocene sapropels studied here. Highly branched isoprenoids are widely used biomarkers for rhizosolenid diatoms (Sinninghe Damsté et al., 2004). Although only five out of > 200 diatom genera are known to produce HBIs (Brown et al., 2014), recent studies show that Pseudosolenia calcar-avis produces HBIs (Kaiser et al., 2016). Rhizosolenoid diatoms, including Pseudosolenia calcar-avis, are the dominant diatoms in the Pliocene-aged sapropel i172 at Site 969 (Kemp et al., 1998), and an important component of the diatom assemblage in the Quaternary sapropels that contain observable diatoms (Kemp et al., 1998; Pearce et al., 1998; Kemp et al., 1999; Moller et al., 2012). The presence of HBIs therefore provides a means by which to test whether the lack of diatom remains in Pliocene sapropels other than i172 at Site 969 is simply due to quantitative opal dissolution. The absence of the predicted, broad suite of HBIs in the MF2 and MF3 samples analysed here (except possible HBI thiolanes in the free lipid fraction of S280-C, which may or may not have a diatom origin) suggests that laminated Pliocene sapropels are not post-dissolution residues of formerly diatom-rich material. It is therefore proposed that mass-sedimentation of colonial pelagic cyanobacteria represents a more likely origin for the organic laminae. Trichodesmium, a genus of planktonic, colonial marine cyanobacteria, occurs throughout the oligotropic tropical and subtropical oceans. They are amongst the most important marine N fixers (Capone et al., 1997) and contribute up to 60% of the total water column phytoplankton standing stock in warm, stratified oligotrophic settings (Carpenter et al., 1997). Trichodesmium colonies, millimetre-scale aggregates comprising 10s to 1000s of individual trichomes, are capable of buoyancy regulation. They migrate up and down the water column in response to changes in light intensity and nutrient availability, and form population maxima at 15-20 m depth. They are best known, however, for their extensive surface blooms (up to at least 2 x106 km2; Capone et al., 1998), which are particularly common under warm, stratified conditions (Carpenter & Capone, 1992) such as those inferred for periods of sapropel deposition during the Pliocene. Trichodesmium blooms can collapse abruptly, either because of viral lysis or autocatalytic programmed cell death (BarZeev et al., 2013; Spungin et al., 2016), the latter generally induced by nutrient stress (i.e. Fe starvation). The innate buoyancy of Trichodesmium, courtesy of numerous robust gas vesicles, coupled to the absence of readily identifiable Trichodesmium detritus in sediment trap material has long led to the view that Trichodesmium-sourced organic matter is almost entirely remineralised within the upper mixed layer, with minimal export of organic detritus to the sea floor (Sellner, 1992). In contrast, a number of recent studies have shown that the programmed cell death response to nutrient stress is expressed as loss of recognisable cellular structure and gas vesicle integrity (Bar-Zeev et al., 2013; Spungin et al., 2016), as well as increased production of extra-cellular polysaccharides. This leads to the formation of several millimetres long aggregates of relatively dense, amorphous organic material with sinking velocities > 200 m per day (Bar-Zeev et al., 2013). These new observations argue for This article is protected by copyright. All rights reserved.

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a rapid transfer of dying and decaying Trichodesmium biomass to depth, with only limited remineralisation within the upper mixed layer. Bloom collapse and programmed cell death triggered by nutrient limitation thus provides a mechanism by which Trichodesmium may contribute to the formation of laminated, organic-rich sediments such as the sapropels. This interpretation is supported by the light δ15N values measured in MF2 samples (−1.8 to −3.0‰; Table 2), indicative of nitrogen fixation by diazotrophs (Karl et al., 2002), and the presence of likely cyanobacterial biomarkers (2α-methylhopanes; Fig. 7I). 2αMethylhopanes were originally interpreted as exclusive biomarkers of cyanobacteria (Summons et al., 1999), although recent work shows that several other bacteria such as αproteobacteria can also produce 2α-methylhopanoids (Rashby et al., 2007; Welander et al., 2010). Genomic data and culture-based work now suggests that only 19% of cyanobacterial genuses synthesize 2-methyl-hopanoids (Ricci et al., 2014), mainly non-marine cyanobacteria. Although it remains unknown whether any of the Trichodesmium species produce 2-methyl-hopanoids, amongst the cultured marine bacteria hopanoids appear to be exclusively synthesized by nitrogen fixing cyanobacteria including Trichodesmium erythraeum (Sáenz et al., 2012). We therefore consider the petrographic features of the organic laminae and the light δ15N in MF2 to be most consistent with a colonial cyanobacterial diazotroph origin for the 2α-methylhopanoids. The discontinuous OM laminae (Fig. 4A) are of similar dimensions to the aggregates of sinking Trichodesmium biomass described in experimental settings (Bar-Zeev et al., 2013). It is proposed that masssedimentation of Trichodesmium following bloom collapse resulted in the accumulation of a large number of individual aggregates at the sea floor, settling over a period of days to weeks and forming a variably thick layer of organic material. While the length scale of individual aggregates is retained, overlap and amalgamation of individual aggregates results in organic zones of variable thickness and increased length, with a wavy to anastomosing appearance. Given the soft, hydrated nature of the amorphous organic material, compaction associated with burial is expected to reduce the thickness of the individual aggregates as well as the composite organic layers by > 90% (Schieber, 2001), producing 10– 60 µm thick composite layers (Fig. 3A) that are comprised of compressed individual aggregates and incorporate drapes of inorganic detritus deposited by pelagic settling or bottom-current reworking over the time-frame of bloom sedimentation (Fig. 3C). Several authors have argued that the light δ15N measured in the majority of Pliocene (and some Pleistocene) sapropels studied to date reflects heightened denitrification under the oxygen-depleted conditions associated with sapropel deposition, favouring nitrogen fixation and increased primary production by cyanobacteria (Meyers & Bernasconi, 2005; Arnaboldi & Meyers, 2006; Gallego-Torres et al., 2011). Although Gallego-Torres et al. (2011) suggested that amplified cyanobacterial primary production is likely to have been associated with bacterial mats in the water column, their assessment is based entirely on bulk geochemical properties and light δ15N in particular. The results presented here show that samples from all microfacies have δ15N values < −1.2‰, consistent with nitrogen fixation, This article is protected by copyright. All rights reserved.

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but only MF2 and (to a lesser extent) MF3 feature the distinct organic laminae and reduced bulk carbonate contents to suggest that colonial cyanobacterial biomass is an important contributor to sapropel organic matter.

Origin of organic matter in non-laminated, high TOC sapropel intervals Not all carbonate-depleted sapropels feature the strong lamination and organic-inorganic couplets suggestive of episodic mass-sedimentation. S280-A and S284-A, for example, are comprised mainly of MF3. Wavy, discontinuous organic laminae of the type observed in MF2 are present but rare and shorter ( 20 µm in size, elongate parallel to bedding, and concentrated in laminae up to 60 µm in length. Where organic laminae are preserved, the elongate pyrite clusters are closely associated with the organic laminae (Fig. 5A). These observations suggest that the first appearance of the elongate, bedding-parallel pyrite clusters marks the delivery of matforming plankton to the sea floor. Microbial breakdown of the mats would have resulted in the establishment of an anoxic blanket at the sea floor as well as the formation of early diagenetic pyrite at the sites of sulphide supply (i.e. adjacent to organic matter as a result of bacterial sulphate reduction; Passier et al., 1999b; Taylor & Macquaker, 2000), well before basinal oxygen depletion progressed sufficiently to permit the formation of water column derived framboidal pyrite. The organic mat components delivered to the sea floor during the first few episodes of mass-sedimentation, before the establishment of an anoxic blanket, was partially removed by oxidation, leaving behind the elongate pyrite framboid


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clusters. It is worth noting that in this example (S282-A) the transition between marl and sapropel is so abrupt that, when viewed in hand sample, it might be mistaken for an erosive contact. It is only by imaging the transition at the appropriate micron-scale resolution that it becomes clear that the abrupt transition reflects a rapid shift in palaeoceanographic conditions that is in stark contrast to the more gradual transitions recorded in some other sapropels. These observations support a model whereby the mass-sedimentation of large, fast-sinking organic aggregates or planktonic mats limits remineralisation and results in the rapid establishment of sea-floor anoxia relative to settings in which a greater fraction of slowsinking organic matter is lost in the water column (Casford et al., 2003; Bianchi et al., 2006). The rapid establishment of sea-floor anoxia is then a function of not only the quantity of export production, but also the plankton type as it influences the temporal distribution of OM export (a rapid pulse following a bloom or water column destabilisation vs a gradual rain of organic debris) as well as the packaging of OM (large, fast-sinking mats vs slower sinking marine snow or smaller aggregates). Local to regional scale variability in water column structure and nutrient availability will therefore be expressed as a patchy spatial distribution of sea-floor anoxia, with the gradual build-up of basinal oxygen depletion (Marino et al., 2007) subsequently producing more uniform sea floor and water column anoxia. While mat-forming diatoms are likely to have played an important role in sapropel S5 (Kemp et al., 1999; Moller et al., 2012), the results presented here suggest that that rapid onset of sea-floor anoxia can equally be a product of mass-sedimentation of pelagic, colonial cyanobacterial biomass. Consequently, early, patchy sea-floor anoxia may be a feature of many of the Pliocene sapropels for which there is little evidence for a significant diatom input and for which oceanographic conditions may not have been conducive to diatom-dominated phytoplankton assemblages. Bioturbation and syndepositional modification of sapropels A sharp decline in TOC and delayed recovery of CaCO3 relative to TOC in the upper part of S280-A is suggestive of burndown and oxidation of OC, resulting in post-depositional truncation of the sapropel (de Lange et al., 2008). The upper portions of all other sapropels investigated here show evidence of bioturbation, both by macrofauna and meiofauna. The widespread occurrence of post-depositional macrofaunal bioturbation (especially Chondrites isp.) in the uppermost section of these Pliocene sapropels has been previously reported (Shipboard Scientific Party, 1996c; Kemp et al., 1998; Löhr & Kennedy, 2015), and reflects the re-establishment of oxygenated bottom-water conditions which permit benthic macrofaunal re-colonisation once sapropel deposition ceases and OM-lean marl deposition resumes. The observation of comprehensive syndepositional reworking of six of the nine intervals studied here (Fig. 2) is a significant new finding, showing that benthic reworking by low-oxygen adapted meiofauna commenced during the waning stages of sapropel deposition. This article is protected by copyright. All rights reserved.

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The thickness of the burrowed interval in each sapropel differs between precessional cycles and between sites (Fig. 2), demonstrating that patterns of bottom-water re-oxygenation and benthic recovery varied through time and space, although the details remain to be determined. S278-B and S282-C are macrofaunally burrowed throughout (Fig. 2), indicating at least transient re-oxygenation of bottom-water throughout their deposition. However, bioturbation is restricted to an upper interval in most sapropels studied. Within this bioturbated interval, gradually decreasing preservation of sediment fabric and lamination towards the upper marl interface coincides with changes to OM preservation style (Fig. 6), beginning with fragmentation of discrete OM laminae (Fig. 6 A-B), increasing ingestion and pelletisation of the sediment (Fig. 6C and D) and, finally, degradation of OM-rich pellets and laminae fragments to form diffuse patches enriched in organic-matter relative to the matrix (Fig. 6E). In a detailed study of S280-B and S282-B, Löhr and Kennedy (2015) identified two classes of OM-rich fecal pellets (Type A and B). Both morphotypes are of benthic meiofaunal origin, representing reworking of sapropels under low-oxygen conditions prohibitive to macrofaunal burrowing organisms, and consistently co-occur with evidence of in situ sediment disruption including OM laminae fragmentation and sediment homogenisation (Fig. 6A). Löhr and Kennedy (2015) interpreted Type A pellets to be of low-oxygen adapted nematode origin, based on the small size and shape of the pellets, as well as the dominance of a nematode meiofauna in comparable modern oxygen-depleted, sulphidic sediments (Pike et al., 2001; Soetaert et al., 2002; Levin, 2003; Steyaert et al., 2007). Low-oxygen adapted small macrofaunal or large meiofaunal polychaetes are abundant in sediments at the extreme end of the dysoxic range (0.2-0.1 ml/l) and are known to produce faecal pellets of size and shape equivalent to Type B pellets (Cuomo & Rhoads, 1987; Cuomo & Bartholomew, 1991; Brodie & Kemp, 1995). In addition, a larger OM-rich fecal pellet type (>> 400 µm) of benthic macrofaunal origin is identified as Type M (Fig. 6F). This morphotype is restricted to heavily macrofaunally bioturbated S282-C and likely reflects deposition and/or reworking under more oxygenated conditions relative to sapropels containing more abundant meiofaunal pellets. The sharp contrast between organic-lean and organic-rich laminae means that the impact of meiofaunal reworking is most obvious in sapropels dominated by MF2, but reworked sediment fabric and meiofaunal faecal pellets are also observed in MF1 and MF3-type sapropels such as S282-C and S284-A. Although there are currently no other documented examples of comprehensive meiofaunal reworking of oxygen-depleted sediments in the geological record, the ubiquity of meiofaunal traces in the sapropels studied here suggests that these organisms were of similar importance for reworking of organic-rich sediments in ancient low-oxygen environments as they are today (Levin, 2003; Giere, 2008). The results presented here further imply that careful analysis of meiofaunal trace abundance in continuous sapropel samples could become a valuable tool in addressing the rate of oceanographic amelioration that is associated with termination of sapropel deposition. This article is protected by copyright. All rights reserved.

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Disruption of lamination and concentration of benthic faecal pellets within specific horizons is commonly interpreted to reflect transient increases in bottom-water oxygen levels allowing restricted benthic activity (Brodie & Kemp, 1995). Differing sensitivity to oxygen depletion and sulphidic conditions implies that the first appearance of 1) meiofaunal (Type A), 2) macrofaunal faecal pellets (Type B) and 3) the later emplacement of Chondrites trace fossils all record environmental thresholds, i.e. more oxygenated or less sulphidic conditions.

CONCLUSIONS Sapropel microfabric preserves a high-resolution record of palaeoceanographic conditions that can be accessed through systematic microbeam imaging and is readily combined with and can help constrain geochemical proxy-based interpretations. Four microfacies are identified. MF1 is interpreted to record periods of diazotroph nitrogen fixation (δ 15N < −1.2‰) and moderately increased primary production by an assemblage of calcareous, siliceous and organic-walled plankton. It is moderately enriched in organic carbon (1–11% TOCcf), mainly preserved within < 15 µm organoclay aggregates, contains > 40% carbonate and has a uniform to massive microfabric. MF1 is present at sapropel bases and throughout low TOC, high carbonate sapropels.

MF2 is carbonate lean (< 40%, often < 5%) but organic-rich (5 to > 25% TOCcf), with a strongly laminated microfabric comprised of alternating 10 - 60 µm thick organic and detrital mineral laminae. MF2 is present within the central, most enriched intervals of high TOC sapropels. The presence of lightly corroded allochems suggests decreased carbonate concentrations may be partially due to increased post-depositional dissolution, but the sharp decrease in carbonate content coinciding with the appearance of the laminated organic fabric in S282-A indicates that this decrease is mainly the result of oceanographic changes resulting in a shift away from calcifying plankton to organic-walled colonial plankton. The characteristic organo-mineral laminae, low δ15N (−1.8 to −3.0‰) and the presence of 2α-methylhopanes (microbial, probably cyanobacterial biomarkers) provide strong evidence for mass-sedimentation of N-fixing colonial pelagic cyanobacteria such as Trichodesmium. The composite nature as well as variable thickness and horizontal continuity of organic laminae suggest that they are formed through the compaction and amalgamation of smaller individual organic aggregates settling to the sea floor following the collapse of Trichodesmium blooms. Furthermore, the presence of framboidal pyrite and discrete OM laminae within 150 µm of the base of sapropel 282-A demonstrates that masssedimentation is associated with abrupt development of bottom-water anoxia, potentially accounting for relatively greater organic enrichment in MF2 intervals. Biomarker evidence indicates organic carbon input from eukaryotic, microbial and higher plant derived organic This article is protected by copyright. All rights reserved.

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matter, in addition to the laminae-forming cyanobacteria. Unlike late Quaternary sapropels, there is no petrographic or biomarker evidence for a mat-forming diatom contribution to these highly organic-rich, laminated intervals. MF3 is moderately organic rich (5–15% TOCcf) and carbonate-lean (< 40%). Like MF2 it is present within central, relatively organic-rich sapropel intervals. Biomarker and δ15N evidence indicates a cyanobacterial but no diatom input, however the uniform to weakly laminated microfabric of MF3 rules out episodic mass sedimentation of colonial cyanobacterial mats. Organic matter is mainly preserved within > 50 µm organomineral aggregates which are interpreted to record increased sedimentation of marine snow and phytodetritus that incorporates and is ballasted by clay minerals. Meiofaunal and/or macrofaunal reworking is the distinguishing feature of MF4, which is present in the upper centimetres of most sapropels. Traces of meiofaunal burrowing include fragmentation of organic laminae and emplacement of organic-rich faecal pellets. These traces are present in six of the nine sapropels studied, and extend to greater depths than macrofaunal burrows, showing that syndepositional meiofaunal reworking of organic-rich sediments by low-oxygen adapted meiofauna is commonplace. The thickness of the burrowed interval in each sapropel differs between precessional cycles and between sites, reflecting changing patterns of bottom-water re-oxygenation and benthic recovery through time and space.

ACKNOWLEDGEMENTS This paper benefited from detailed comments by two reviewers and the Editorial Office. The research used samples and data provided by the Ocean Drilling Program (ODP). The successor program (IODP) is sponsored by the U.S. National Science Foundation (NSF) and participating countries under management of Joint Oceanographic Institutions (JOI), Inc. We thank the Australian Research Council (DP110103367 and LP120200086 to MJK) and the Australian and New Zealand IODP Consortium (ANZIC) which provided Legacy/Special Analytical Funding for this study. ANZIC is supported by the Australian Government through the Australian Research Council’s LIEF funding scheme (LE140100047) and the Australian and New Zealand consortium of universities and government agencies. We thank Alex Wülbers of the Bremen Core Repository for core sampling. HX acknowledges support from Macquarie University and the China University of Geosciences (Beijing). We thank Alex Holman, Mark Tran and Anthony Gurlica for help with the Raney nickel experiments, and Mark Rollog (University of Adelaide) for the stable isotope analyses. The authors have no conflict of interest to declare.


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Accepted Article

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Accepted Article

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Accepted Article

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FIGURE CAPTIONS Figure 1: Topographic and bathymetric map of the eastern Mediterranean region, generated in Ocean Data View (Schlitzer, 2017). Red dots indicate location of ODP drilling sites discussed here. Figure 2: %TOC (solid black), %CaCO3 (grey squares and dashed line) and dominant microfacies (determined by SEM/BSE) in three Pliocene sapropel cycles from ODP Sites 964, 969 and 967. Red stars mark organic geochemical analyses (Table 4), green stars mark depths of stable isotope analyses (Table 2). Representative photomicrographs of each microfacies (MF1 to MF4) are presented in Figures 3, 4 and 6, respectively. Also shown for each hole are a photographic log, major macrofeatures, depth of samples imaged by SEM, and distribution of Type A, B and M faecal pellets. Figure 3: Representative SEM BSE images of Microfacies 1. (A) Sample 967/B/9/6/71-72, 80.01 mbsf. Microfacies 1 is characteristic of the basal marl-sapropel interface, and is characterised by a homogeneous microfabric with abundant biogenic calcareous allochems (primarily foraminifera and coccoliths) and a low abundance of organic carbon that is concentrated in organo-clay aggregates (arrows). (B) Sample 967/B/9/6/117-118, 80.47 mbsf. Greater abundance of organic carbon relative to (A), abundant coccoliths. (C) Sample 969/A/6/6/104-105, 53.98 mbsf. Higher magnification image showing organo-mineral aggregate nature of organic domains and abundance of biogenic calcareous material. (D) Sample 967/B/9/6/107-108, 80.37 mbsf. Microfacies 1, weakly laminated. Note higher abundance of OC relative to (A) and (B), present as organoclay aggregates but also as thin, discontinuous laminae (yellow arrows). Abundant calcareous microfossil debris, including coccoliths (white arrows) and foraminifera tests (black arrows). (E) Sample 967/B/9/6/116117, 80.46 mbsf. Abundant calcareous biogenic debris, particularly coccoliths, inorganic detrital minerals, organo-clay aggregates and intermingled amorphous organic material. (F) Sample 967/B/9/6/116-117, 80.46 mbsf. Higher magnification image of (E), showing organoThis article is protected by copyright. All rights reserved.

mineral aggregate nature of organic-rich domains and abundant coccoliths.

Accepted Article

Figure 4: Representative SEM BSE images of Microfacies 2 (A to C) and Microfacies 3 (D&E). (A) Sample 964/A/9/5/35-36, 79.65 mbsf. Discrete OM laminae (dark) are concentrations of OM largely devoid of detrital minerals, interpreted to result from mass sedimentation of colonial phytoplankton. Interbedded organic-lean laminae (light) represent normal background sedimentation, and comprise mainly detrital clays. Note discontinuous nature and variable thickness of individual organic laminae. Yellow arrows mark organic laminae terminations. (B) Enlarged from previous. Silt-size quartz (orange) and feldspar (green), distinguished by elemental mapping (EDX), are interpreted to be of aeolian origin and are mainly present within mineral laminae. (C) Sample 964/A/9/5/34-35, 79.64 mbsf. Higher magnification image revealing the composite nature of organic laminae. Yellow arrows mark junctions between amalgamated organic mat components and components separated by mineral drapes. (D) Sample 964/A/9/5/90-91, 80.20 mbsf. Typical example of Microfacies 3. Weakly laminated microfabric, characterised by rare discrete organic laminae (yellow arrows). The bulk of the OC is diffusely dispersed through the sediment, closely intermingled with the mineral matrix. Abundant framboidal pyrite is indicative of anoxic seafloor or porewater conditions; calcareous microfossil debris is absent. (E) Sample 964/A/9/5/90-91, 80.20 mbsf. Microfacies 3, organo-mineral matrix comprising organo-clay aggregates, mica, quartz, feldspar and diagenetic framboidal pyrite. Figure 5: (A) Sample 964/A/9/5/37-38, 79.67 mbsf. Backscatter electron image with EDS elemental map of Ca (red), Al (light blue), Si (light brown) and S (yellow) overlaid. Base of S282-A, showing interface between marl (bottom) and sapropel (dashed line B1), characterised by sharp decline in calcareous biogenic material and appearance of organoclay aggregates. Increased abundance of early diagenetic framboidal pyrite above the dashed line marked B2 indicates a sudden change to sea-floor redox conditions. Framboidal pyrite is concentrated in bedding-parallel laminae (yellow arrows). The organo-aggregate and framboidal pyrite interval continues until the appearance of discrete organic laminae above the dashed line marked B3. The organic laminae (black arrows) are associated with bedding-parallel laminae of framboidal pyrite (yellow arrows). (B) Sample 969/A/6/7/43-44, 54.87 mbsf. Transitional sample between Microfacies 1 and 2. Laminated microfabric due to replacement of organo-mineral aggregates by discrete OM laminae. However, nektonic faecal pellets containing calcareous debris (dashed white outline) show that calcareous plankton remained an important component of the phytoplankton assemblage until 54.85 mbsf. (C) Sample 969/A/6/7/41-42, 54.85 mbsf. Microfacies 2 showing discrete OM laminae and abundant framboidal pyrite. (D) Sample 967/B/9/6/71-72, 80.01 mbsf. Typical example (arrow) of structured organic particle. Similar material was observed in most samples, but is only a quantitatively significant contributor to TOC in the marls. Figure 6: Representative SEM BSE images of Microfacies 4A (A to D) and Microfacies 4B (E & F). (A) Sample 969/A/6/6/142-143, 54.36 mbsf. Microfacies 4A, base of the bioturbated


Accepted Article

interval of sapropel S280-B. OM laminae fragments (white arrows) and meiofaunal faecal pellets (yellow arrows) are marked. The systematic co-occurrence of laminae fragments showing features indicative of physical reworking and meiofaunal fecal pellets indicate that meiofaunal reworking resulted in fragmentation of formerly more continuous discrete OM laminae (see also Löhr & Kennedy, 2015). (B) Sample 964/A/9/5/31-32, 79.61 mbsf. Deformed fragments of formerly continuous, discrete OM laminae with meiofaunal faecal pellets (arrows). (C) Sample 969/A/6/7/38-39, 54.82 mbsf. In the upper parts of most sapropels, OM is concentrated in meiofaunal benthic faecal pellets 300 µm) were only observed in sapropel S282-C. Type M pellets (two example outlined, others marked by white arrows) are less organic-enriched than most Type A and Type B pellets, and hence do not show the distinct compositional contrast to the mineral matrix, likely reflecting a greater admixture of inorganic mineral material due to a larger mouth diameter in the macrofauna relative to the meiofaunal nematodes and polychaetes. Figure 7: (a) Total ion chromatograms of the aliphatic fractions of sapropels S284-A, S280-C and S284-C. (b) Partial mass chromatograms (m/z 57, 179, 210, 238, 346, 348) of S284-C, showing the distribution of C25 highly branched isoprenoid (HBI), C25 HBI-dienes, C25 HBItrienes and C25 HBI bicyclic compounds a and b relative to n-alkanes. (c) Mass spectra of compound a. (d) Mass spectra of compound d. (e) Partial mass chromatograms (m/z 57, 115, 380) of S280-C showing the distribution of C25 HBI thiolanes relative to n-alkanes. (f) Mass spectra of thiolane peak j. (g) Partial mass chromatograms (m/z 191) for sapropels S284-A, S280-C and S284-C. (h) Partial mass chromatograms (m/z 215) for sapropels S284-A, S280-C and S284-C. (i) Partial m/z 205 mass chromatogram of the aliphatic fraction of the Raney nickel desulphurised polar fraction of sapropel S284-C, showing the presence of significant amounts of 2α-methylhopanes, which were detected in all three microfacies (Table 4). Peak identifications for (g): 1 = 17β-22,29,30-trisnorhopane; 2 = C29 norneohop13(18)-ene + C29 αβ norhopane; 3 = C30 hop-17(21)-ene; 4 = C30 αβ hopane; 5 + 6 = C30 neohop-13(18)-enes?; 7 = C29 ββ norhopane + C30 βα moretane; 8 = C30 pentacyclic triterpenes; 9 = C30 ββ hopane; 10 = C31 ββ homohopane. Peak identifications for (h): 1 = C27 sterene; 2 = C28 steradiene; 3 = C27 steradiene + C28 stertriene; 4 = C28 sterene; 5 = C28 sterene; 6 = C28 steradiene; 7 = C27 sterene + C28 steradiene; 8 = C29 sterene; 9 = C29 steradiene.


TABLES

Accepted Article

Table 1: Sapropel intervals characterised for this study*. Sapropel ID

Leg

S278-A

160 964 A

9H

S280-A

160 964 A

9H

Sapropel interval

i-Cycle

Age (Ma)

4

73-87(?) cm

278

2.900 Ma

4

136-139 cm

280

2.921 Ma

Site Hole Core Section

Water depth

3658 m

S282-A

160 964 A

9H

5

31-37 cm

282

2.943 Ma

S284-A

160 964 A

9H

5

89-95 cm

284

2.965 Ma

S278-B

160 969 A

6H

6

99-106 cm

280

2.900 Ma

S280-B

160 969 A

6H

6/7

140-5 cm

282

2.921 Ma

S282-B

160 969 A

6H

7

36-47 cm

284

2.943 Ma

S280-C

160 967 B

9H

6

9-25 cm

280

2.921 Ma

S282-C

160 967 B

9H

6

56-71 cm

282

2.943 Ma

S284-C

160 967 B

9H

6

103-118 cm

284

2.965 Ma

* Insolation (precession)-cycle and age after Lourens et al. (1996) and Emeis et al. (2000)


2200 m

2555 m

Accepted Article

Table 2: δ15N and δ13Corg of the most organic-rich samples of each sapropel (sampling depths shown in Fig. 2). Analytical error is 0.45 and 0.1‰ on δ15N and δ 13Corg values, respectively. Sample

Sapropel

δ15N Microfacies (‰)

δ 13Corg (‰)

964/A/9/4/135136

S280-A

MF3

−1.3

−22.5

964/A/9/5/34-35

S282-A

MF2

−2.7

−23.4

964/A/9/5/91-92

S284-A

MF3

−2.1

−23.4

969/A/6/6/101102

S278-B

MF4B

−1.2

−23.6

969/A/6/6/149150

S280-B

MF2

−2.6

−23.6

969/A/6/7/41-42

S282-B

MF2

−1.8

−24.4

967/B/9/6/18-19

S280-C

MF2

−3.0

−23.5

967/B/9/6/61-62

S282-C

MF4B

−2.2

−23.6

967/B/9/6/111112

S284-C

MF1

−3.1

−23.4


Table 3: OM classes identified in Pliocene sapropels from ODP Sites 964, 969 and 967 Origin

Description & Interpretation

Discrete OM laminae (Fig. 4 A-C; Fig. 5C)

Primary

Organic laminae and lenses, discontinuous at the mm scale, often wavy or branching, deformed around large grains and early accumulations of authigenic minerals. Largely free of detrital mineral components, but commonly contain authigenic pyrite and carbonate. Thickness > 10 µm, commonly 20-40 µm, but lenses can reach ≈ 100 µm. Generally clear boundaries to adjacent detrital material, although the transition may appear diffuse where the laminae are < 20 µm thick.

Diffuse OM laminae (Fig. 4D)

Primary

Similar to discrete organic laminae, but contain an appreciable quantity of detrital materials, and are consequently less enriched in OM. Grade diffusely into the adjacent mineral matrix. Diffuse laminae may contain patches or lenses of discrete OM. They are often thinner than discrete OM laminae, and can be difficult to distinguish from OM that is diffusely mixed through the sediment matrix rather than more concentrated in diffuse OM laminae.

Organoclay aggregates (Fig. 3 & Fig. 4 D&E)

Primary

Aggregates of clays and organic matter. These can be of varying size, 5-20 µm are most common in MF1 whereas larger aggregates with less distinct boundaries are typical of MF3. Organoclay aggregates are morphologically diverse, but irregular outlines and diffuse to wispy boundaries are most common. Aggregates with irregular, sharp outlines are also common. Most aggregates are heterogeneous with varying amounts of OM and clays in the aggregate centre vs the outer areas.

Discrete organic detritus (Fig. 5D)

Primary

Palynomorphs such as pollen grains and algal spores, as well as phytodebris. While present in most samples, discrete organic detritus only represents a quantitatively significant contribution to TOC in OC-lean marls.

Fragmented OM laminae (Fig. 6)

Bioturbated

Variably sized, irregularly shaped, commonly elongate zones of OC enrichment with clear boundaries. They contain varying ratios of OC relative to detrital and authigenic phases, depending on the presence of discrete or diffuse OM laminae in the sapropel. OM laminae fragments are confined to bioturbated intervals, are always associated with faecal pellets and are interpreted as discrete organic laminae physically disrupted and fragmented by benthic infauna but, unlike faecal pellets, have not been ingested.

Faecal pellets (Fig. 6)

Bioturbated

Organic-rich faecal pellets of benthic meiofaunal and macrofaunal origin. These have sharp, defined boundaries to the adjacent matrix, with different fabric and particle orientation. Varying amounts of OC

Accepted Article

Type


Accepted Article

Large OM patches (Fig. 6E)

relatively to inorganic phases, but high OC/low mineral pellets are limited to sapropels dominated by discrete OM laminae. Three morphotypes are observed: Type A, round to ovoid pellets 15-35 (if sectioned across the long axis) and 35-70 µm in size (if sectioned along the long axis); Type B, 60-100 and 100-300 µm length (across vs along long axis); Type M, ovoid pellets mostly >> 400 µm in length. Type A occurs throughout meiofaunally bioturbated intervals, while Type B is mostly restricted to the uppermost cm of these intervals. Type M pellets were observed in S282C only. Bioturbated

Zones of OC enrichment relative to the matrix, with indistinct irregular to oval shapes and diffuse to wispy outlines grading into the matrix. These organic-rich patches are confined to bioturbated intervals and co-occur with faecal pellets and organic laminae fragments. They are most common in the heavily bioturbated portions of a sapropel, and are interpreted as degraded organic laminae fragments and faecal pellets, particularly of macrofauna rather than as primary organoclay aggregates.


Table 4: Molecular geochemistry of sapropels*. S284-A, 964, A, 9H, 5

S280-C, 967, B, 9H, 6

S284-C, 967, B, 9H, 6

Interval (cm)

92 - 93

16 - 20

109 - 115

Depth (mbsf)

80.22

79.46 - 79.49

80.39 - 80.44

Microfacies

MF3

MF2, 4A

MF1

Extractability (mg / g)

9.9

37.0

6.6

Pr / Ph

0.61

0.60

0.80

Pr / n-C17

0.22

0.38

0.40

CPI22-32

2.6

1.5

2.5

TAR

11.1

7.8

9.8

ACL25-33

29.6

28.8

29.8

Lycopane / n-C31

0.18

0.60

0.46

C29-C31 ββ hopanes / C30 neohop-13(18)-enes

5.1

5.1

2.6

C30 hop-17(21)-ene / C30 neohop-13(18)-enes

0.31

1.33

0.21

C27 : C28 : C29 sterenes

1 : 3.6 : 3.3

1 : 0.8 : 3.1

1 : 2.8 : 6

C31 2α-Me / ( C31 2α-Me + C30 αβ hopane) (free lipid fraction)

0

0

0

C32 2α-Me / ( C32 2α-Me + C31 αβ hopanes) (free lipid fraction)

0

0

0

C31 2α-Me / ( C31 2α-Me + C30 αβ hopane) (sulphurbound fraction)

0.38

0.35

0.38

C32 2α-Me / ( C32 2α-Me + C31 αβ hopanes) (sulphur-bound fraction)

0.23

0.15

0.17

Accepted Article

Sapropel ID, Site, Hole, Core, Section

*

Note that the marl interval underlying S284-C (80.5-80.57 mbsf) was also extracted. Data from this interval is not presented as it was very lean. Pr = pristane; Ph = phytane; CPI = carbon preference index; TAR =terrigenous / aquatic ratio (n-C27 + n-C29 + n-C31) / (n-C15 + n-C17 + n-C19); ACL = Average chain length (25(n-C25) + 27(n-C27) + 29(n-C29) + 31(n-C31) + 33(n-C33)) / (n-C25 + n-C27 + n-C29 + n-C31 + n-C33); 2α-Me = 2α-Methylhopane.


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